Distinct roles for PARP-1 and PARP-2 in c-Myc-driven B-cell lymphoma in mice

Dysregulation of the c-Myc oncogene occurs in a wide variety of hematologic malignancies, and its overexpression has been linked with aggressive tumor progression. Here, we show that poly (ADP-ribose) polymerase 1 (PARP-1) and PARP-2 exert opposing influences on progression of c-Myc-driven B-cell ly...

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Detalles Bibliográficos
Autores: Galindo-Campos, M. A., Lutfi, Nuria, Bonnin, S., Martínez, C., Velasco-Hernández, Talia, García-Hernández, V., Martín Caballero, Juan, Ampurdanés, Coral, Gimeno, R., Colomo, L., Roué, Gaël, Guilbaud, G., Dantzer, Françoise, Navarro Medrano, Pilar, Murga, Matilde, Fernández-Capetillo, Óscar, Bigas, A., Menéndez, Pablo, Sale; J. E.
Tipo de recurso: artículo
Estado:Versión aceptada para publicación
Fecha de publicación:2022
País:España
Institución:Consejo Superior de Investigaciones Científicas (CSIC)
Repositorio:DIGITAL.CSIC. Repositorio Institucional del CSIC
OAI Identifier:oai:digital.csic.es:10261/278133
Acceso en línea:http://hdl.handle.net/10261/278133
Access Level:acceso abierto
Palabra clave:Animals
Carcinogenesis / genetics
DNA Damage
Gene Deletion
Gene expression regulation
Neoplastic Lymphoma
B-Cell / genetics
Mice
Mice, Knockout
Poly (ADP-Ribose) Polymerase-1 / genetics
Poly(ADP-ribose) Polymerases / genetics
Proto-Oncogene Proteins c-myc / genetics
Descripción
Sumario:Dysregulation of the c-Myc oncogene occurs in a wide variety of hematologic malignancies, and its overexpression has been linked with aggressive tumor progression. Here, we show that poly (ADP-ribose) polymerase 1 (PARP-1) and PARP-2 exert opposing influences on progression of c-Myc-driven B-cell lymphoma. PARP-1 and PARP-2 catalyze the synthesis and transfer of ADP-ribose units onto amino acid residues of acceptor proteins in response to DNA strand breaks, playing a central role in the response to DNA damage. Accordingly, PARP inhibitors have emerged as promising new cancer therapeutics. However, the inhibitors currently available for clinical use are not able to discriminate between individual PARP proteins. We found that genetic deletion of PARP-2 prevents c-Myc-driven B-cell lymphoma, whereas PARP-1 deficiency accelerates lymphomagenesis in the E¿-Myc mouse model of aggressive B-cell lymphoma. Loss of PARP-2 aggravates replication stress in preleukemic E¿-Myc B cells, resulting in accumulation of DNA damage and concomitant cell death that restricts the c-Myc-driven expansion of B cells, thereby providing protection against B-cell lymphoma. In contrast, PARP-1 deficiency induces a proinflammatory response and an increase in regulatory T cells, likely contributing to immune escape of B-cell lymphoma, resulting in an acceleration of lymphomagenesis. These findings pinpoint specific functions for PARP-1 and PARP-2 in c-Myc-driven lymphomagenesis with antagonistic consequences that may help inform the design of new PARP-centered therapeutic strategies, with selective PARP-2 inhibition potentially representing a new therapeutic approach for the treatment of c-Myc-driven tumors.